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Ryan M J (2009) Communication in Frogs and Toads. In: Squire LR (ed.) Encyclopedia of Neuroscience, volume 2, pp. 1159-1166. Oxford: Academic Press.

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Communication in Frogs and Toads 1159

Communication in Frogs and Toads

M J Ryan , University of Texas, Austin, TX, USA Origin and Mechanisms of Sound

Modern frogs produce sound by expelling air from the

lungs through the larynx. The larynx sits on a ring of Introduction cricoid cartilages on the hyoid plate. It consists of two arytenoid cartilages that close on the top of the larynx Anurans, commonly known as frogs and toads, are and which, inside, support a pair of vocal folds, one among the most vociferous of animals. Their noctur- extending across the interior of each arytenoid cartilage nal cacophony characterizes many landscapes and (Figure 2). As air passes through the lungs, it vibrates the seasons, such as vernal ponds in the temperate-zone vocal folds, and it is this vibration that brings about spring and rainforests in the neotropical wet season. the pressure fluctuations that are perceived as sound. This serenade is an annual mating ritual. Males The mass and tension of the vocal folds are primarily broadcast long-distance calls to attract females and responsible for the spectral properties of the emitted repel other males, and females use these calls to sound. In some species such as the tu´ngara frog, Phy- choose mates. salaemus pustulosus, masses can be added to the vocal Anuran sexual communication has emerged as an cord to decrease its fundamental frequency of vibration especially tractable system for integrative studies of (Figure 2). The opening and closing of the arytenoid brain, behavior, and evolution. There are about 5000 cartilages can shape the waveform of the sound. species of frogs, and the long-distance mating or The frog’s larynx opens into the floor of the mouth. advertisement calls is their most obvious signal. In many frogs, there are vocal slits in the mouth that

A caveat, however, should be implicit throughout open into a vocal sac that expands as the call is pro- this account. Anurans encompass incredible diversity duced. The vocal sac is usually quite thin and enhances in communication, and this article merely describes the coupling of the sound to the environment. The some of the more common themes in the manner in vocal sac seems not to be a cavity resonator; in Pseu- which these animals acoustically communicate with dacris crucifer and Physalaemus pustulosus,thedomi- each other. nant frequency of the call does not change when males Frogshave a variety of calls that communicate call in a helium–oxygen mixture (as it would if it were a different types of information. These include long- resonator, since frequency is the speed of sound divided distance mating or advertisement calls, territorial by wavelength, and the speed of sound varies with calls, aggressive calls, encounter calls, distress calls, medium density while the emphasized wavelength of release calls, short-distance courtship calls, and rain a resonator remains constant). In an unusual case of calls. Not all species produce all these call types, and sound coupling, the large external tympanic membrane most have a rather modest repertoire. One glaring of the male bullfrog couples sound to the environment. exception, however, is Boophis madagascariensis Thus these frogs call as well as hear through their ears. (Rhacophoridae), a frog found in the forests of east- Frogs can also make use of the external environment ern Madagascar. Call notes produced by these males to enhance signal coupling. A treefrog in Malaysia, have been classified into 28 types (Figure 1), the Metaphrynella sundana, for example, calls in tree largest known call repertoire of any anuran, although holes and varies the call’s dominant frequency to little is known of the function of these call types. match the hole’s resonance. Most studies of anuran communication concen- Vocal sacs can be quite varied in appearance trate on one call in the frog’s repertoire, the mating (Figure 3) and have other functions besides acoustic call, which mediates social interactions during mate coupling. Air is recycled between the vocal sac and attraction. Because the mating call figures so strongly the lungs; thus buccal pumping is not required to in female mate choice, this dyadic interaction is criti- inflate the lungs after each call. This saves energy, in cal in ensuring successful reproduction; furthermore, P. pustulosus at least, and allows males to call at it can drive speciation between populations by pro- a faster rate, which is more attractive to females. moting mate recognition of only local populations, A male frog’s large pulsating vocal sac can also serve and female preferences among appropriate mates can as a visual cue. In both Hyla squirella and P.pustulosus, cause the evolution of increasingly elaborate signals the vocal sac is a visual cue that further increases the through the action of sexual selection. attractiveness of the acoustic cue to the female.

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1160 Communication in Frogs and Toads

abc d efgij h

400 nm 8 50 nm 400 nm

(kHz) Frequency

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8 400 nm

(kHz) Frequency

0 Figure 1 Waveforms and sound spectrograms of representative call notes produced by males of Boophis madagascariensis: a, toc note; b, short click note; c, short rip note; d, loud click note; e, tone-like note with a fundamental frequency of 670 Hz; f, long rip note; g, Æ creak note; h p, iambic (I) notes with increasing numbers of pulses: (h) I2, (i) I3, ( j) I4, (k) I5, (l) I6, (m) I7, (n) I8, (o) I9, (p) I23. Except for I21, all notes from I10 to I22 were also produced, but are not illustrated. Analysis filter bandwidth: a and b: 300 Hz; c and d: 150 Hz; all Æ other spectrograms: 59 Hz. Ambient recording temperatures were in the 18–22 C range. Timescale for sound spectrograms a e has been magnified to provide increased temporal resolution. Reproduced from Narins PM, Lewis ER, and McClelland BE (2000) Hyper- extended call note repertoire of the endemic Madagascar treefrog Boophis madagascariensis (Rhacophoridae). Journal of Zoology (London) 250: 283–298, with permission from Blackwell Publishing.

Receivers the water. But there is little doubt that the hearing of frogs has primarily evolved to enhance sexual In frogs, more so than in most other animals, the neural communication. properties of the receiver are inextricably linked to All anurans have two inner ear organs, the amphib- sexual communication. This is most clearly illustrated ian papilla (AP) and the basilar papilla (BP), that are by Capranica’s matched-filter hypothesis, which sug- sensitive to airborne sound. Furthermore, the saccule gests that among species, the tuning of two auditory is sensitive to surface vibrations. In some frogs, such end organs matches the distribution of spectral energy as the white-lipped frog, Leptodactylus albilabris, the in the mating call. surface vibrations that result from the vocal sac’s The Auditory System striking the ground are perceived by the receiver as a salient part of the vocal display. Most research has concentrated on how the frog’s auditory system decodes the mating call. But frogs Tympanic membrane and middle ear Frogs lack pin- do attend to other sounds. Reed frogs (Hyperolius nae. Some frogs, such as some members of the genus nitidulus) in Africa can hear the roar of fire rolling Atelopus, lack both external ears and middle ears, even across savanna, and they respond by jumping into though these frogs clearly communicate acoustically.

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Communication in Frogs and Toads 1161

Figure 2 The laryngeal morphology of the tu´ngara frog. The arytenoid cartilages are in yellow, the cricoid cartilage in red, the fibrous masses in blue, the vocal folds in white, the bronchi in green, and the lungs in pink. (a) Approximate position of the larynx and lungs in the calling frog. (b) Simplified illustration of the larynx without bronchi or lungs. (c) A view of the larynx from the lungs showing the intrusion of the fibrous masses into the bronchi. (d) A medial section of the larynx showing the attachment of the fibrous mass to the vocal fold. Reproduced from Gridi-Papp M, Rand AS, and Ryan MJ (2006) Complex call production in tu´ngara frogs. Nature 441: 38, with permission.

Figure 3 A sample of the diversity of vocal sacs of frogs. Clockwise from top left: African reed frog (Hyperolius bayoni), from www. exploratorium.edu/frogs/mainstory/hbayoni.html ; Amazonian arboreal frog (Phrynohyas coriacea), from Hofrichter R (ed.) (2000) Ency- clopedia of Amphibians (p.162). Toronto, Canada: Key Porter Books; squirrel treefrog (Hyla squirella), American toad (Bufo americanus), and carpenter frog (Rana virgatipes), all from www.naturesound.com.

In most frogs, however, there is a tympanic membrane Inner ear Both the AP and BP are involved in on the outside of the head and a collumella in the sound detection, but the details of these structures middle ear, which transduces outer ear vibrations to are quite different. The AP has about 1000–1500 the oval window of the inner ear. This vibration causes hair cells in the bullfrog, Rana catesbeiana, and its disturbance of the inner ear fluid, which in turn causes membrane is tonotopically organized. The AP is most movements of membranes in both the AP and BP. sensitive to lower frequencies, from a few hundred Hz

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1162 Communication in Frogs and Toads to about 1500 Hz. The AP usually has two peaks of some behavioral evidence to suggest that the ultrasonics frequency sensitivity. In the bullfrog, for example, influence the male’s calling behavior, and neurophysio- there is a lower peak of about 100–200 Hz and a logical studies of evoked potentials show clearly that mid-frequency peak of about 500–600 Hz. Neurons the frogs can hear these sounds. most sensitive to the lower-frequency peak exhibit Central Processing two-tone suppression, but this is not true of the mid-frequency peak. The BP, by comparison, has Much of the integration of acoustic information from fewer hair cells, 60–90 in the bullfrog, and is not the two inner ear organs takes place in the torus tonotopically organized. The hair cells in the BP tend semicircularus, a large auditory nucleus in the mid- to be most sensitive to the same frequency, about brain homologous to the mammalian inferior collicu- 1400–1500 Hz in bullfrogs. lus. Electrophysiological studies show more complex The tuning of the AP and BP of a species tends to processing in the torus than in the inferior colliculus: coincide with the frequency peaks in its mating call. Some cells respond to simple stimuli such as tones, In frogs that call in a narrow frequency range, there is whereas others respond only to specific combinations a match between the tuning of either the AP or the BP of sounds such as those found in the species’ mating and call frequency, whereas in frogs that call over a call. Studies using electrophysiology and immediate wider frequency range, the tuning of both end organs early gene (IEG) expression have mapped spatial var- match frequency peaks in the call. A recent review of iation in auditory activity in the torus in response to these data showed that species variation in the carrier call variation and found evidence for parallel proces- frequency of calls explains 82% of the variation in the sing of different aspects of acoustic stimuli. In tu´ngara tuning of the inner ears organs (Figure 4). frogs, combining IEG expression measures throughout At least one species of frog, the concave-eared tor- the torus provides sufficient information to discrimi- rent frog (Amolops tormotus), uses ultrasonics in nate between conspecific and heterospecific calls as communication. This Chinese frog calls near rushing well as between simple and complex conspecific calls. streams, and the ultrasonics are above most of the Further acoustic processing takes place in thalamic spectral energy in the background noise. There is auditory nuclei. As with the torus, parallel processing occurs here. Lesioning studies in gray treefrogs show 6 r 2 = 0.82 that female phonotaxis requires a functioning torus semicircularis but not dorsal thalamus. Dorsal thalamic nuclei might function in motivation or attention

AP BP relative to phonotactic readiness. 4 Thalamic and midbrain auditory nuclei have ana- tomical projections to various forebrain regions that

receive inputs from multiple sensory modalities. Electro- physiological and metabolic measures have found

2 acoustic responsiveness in auditory system targets in the hypothalamus and telencephalon. In the tu´ ngara

frog, IEG analyses have also shown that correlated patterns of neural activity within the hypothalamus vary with signal salience. Lesioning dopaminergic

Carrier frequency of advertisement call (kHz) 0 0246 cells in the green treefrog, Hyla cinerea, impaired Auditory system responsiveness: phonotaxis behavior, and the residual phonotaxis Estimated frequency at lowest threshold (kHz) behavior correlated with the number of surviving

Figure 4 Scatter diagram of the spectral peaks of the advertise- dopamine cells in one region of the hypothalamus. ment calls of 24 anurans (plus three populations of one species) These IEG and lesioning studies suggest the existence versus estimates of the best excitatory frequency of the peri- of social neural networks that integrate auditory and pheral auditory system. Green circles represent data in which motivation information and influence the motor out- closed-field stimulation was used in the neurophysiological recordings, and gray symbols show data in which free-field stimu- puts that constitute phonotaxis. lation was used. Squares represent low frequencies attributed to the amphibian papilla (AP), and circles represent sensitivities attributed to the basilar papilla (BP). The white and gray back- Behavior and Evolution grounds estimate the range of frequency sensitivities of the AP and BP, respectively. Modified from figure 7.1 of Gerhardt HC and Other Modes and Multimodal Communication Schwartz JJ (2001) Auditory tuning and frequency preferences in anurans. In: Ryan MJ (ed.) Anuran Communication, pp. 73–85. Frogs communicate in modalities besides the auditory Washington, DC: Smithsonian Institution Press. one. Tadpole social behavior, for example, is strongly

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Communication in Frogs and Toads 1163

Figure 5 Visual signaling in Phrynobatrachus kreftii. Female (above left) and male without vocal sac expansion (above right), with partly expanded vocal sac (below right), and with fully expanded vocal sac (below left). Note the bright yellow subgular region of the male. Photograph by Walter¨ dl Hoat Zigi River (Amani Nature Reserve), Tanzania. From figure 1 of ¨ dlHirshmann W (2006) W Visandu alHo signaling in Phyrnobatrachus krefftii Boulenger, 1909 (Anura: Ranidae). Herpetologica 62: 18–27.

influenc ed by olfactor y cues. In ag gregationsdiurnal of patad- tterns. Most frogs call at night, but some, poles of the American toad, Bufo american usp e,r hasiblingps m osts notably poison frogs, call during the day. are more lik ely to be found in proxim Thityer e toar e onealso diel patterns as most frogs do not call another than to nonsibling s. These and manyfr omspecies dusk to dawn. In the El Verde forest of Puerto of tadpo les can discrimi nate sib from nonsibRico, wanhi chd is rich in frogs of the genus Eleuthero- pater nal half-sib from sib using odor cues thatd a becomc t yl e us , there is acoustic partitioning of frequencies incor porate d into the jelly mat rix of the wnest.ithin choruses, but when call frequencies are similar Visual cues a re important in sexual comm beunicationtween sympatric species of Eleutherodactylus,they in many diurnal frogs, such as the poison frogscall atof dtheifferent times at night. family Dendrob atidae. Dendro bates pum ilio onTempor dif- al patterni ng also occurs at a fine r scal e. ferent island s in the Bocas del Tor o regionOnly of aPanama few species of frogs , such as the neotropi cal show striki ng differen ces in color patternSmilisca , andsila , synchro nize their callin g. In this case, female s’ prefe rence for local mal es is strongsynchroni ly influ-zation makes the frogs less suscep tible to enced by visual cues. Other diurnal frogs ,predat such ionas by the frog- eating bat Trachops cirrho sus.

Hylod es and Atelopus zetek i, have dynamicMost visual frogs, howev er, alternat e calls. Call alternat ion displays, waving thei r limbs at other frogs inusually a stereo-occu rs withi n a small neighbor hood, an d typed pattern. Bot h frogs live near rushi ngthus, streams, the summ ed a coustic outp ut of a n enti re chorus where the backgrou nd noise mi ght not be cancondu lack cive any easily discerni ble structure . Some of to acoust ic communic ation when rain is abuthe ndant.best studies of these types of interact ions have The vocal sac can also serve as a visua beenl cue. con Mducted ale with the neotropi cal treefrog s Hyla poison frogs , Epipedob ates femoral is, atta microceck models phala , H. phlebod es, and H. ebracc ata . Males with pulsating vocal sacs. In a diurnal frogof thesefrom species adjust thei r pa tterns of calli ng to Tanzani a, Phrynob atrachu s krefftii , malesavoid silently overl ap of calls with co nspecifics as well as inflat e thei r bright yello w vocal sacs as similaa visuar- so l undsignal in g c o ng enerics. Males of b oth Eleuth ero-

( Figure 5). The vocal sac can also contributeda tocty lusmulti- coqui and Hyperolius b roadley i have espe- modal commu nication. cially impressive abilities to produce c alls in ga ps between the ca lls o f other m ales. Male Calling In many species of chorusing frogs, nonrandom

Most frogs form cho ruses to vocal ly advertisspacing e of callingfor males occurs whether or not males female s. As choruse s are associ ated with defend reproduc territories - such as oviposition sites. In some tion, there are seasona l patterns; choru ses formspecies, in suchthe as the neotropical Eleutherodactylus breedi ng season but not out of it. Therediastema are andalso the North American spring peeper,

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1164 Communication in Frogs and Toads

Pseudacris crucifer, the amplitude of the nearest that calls of the two species evolve to be more different neighbor’s call, rather than the neighbor’s physical in sympatry. This is the case in two species of chorus distance, appears to be more important in determin- frogs in Florida, Pseudacris nigrita and P. ferriarum. ing nearest-neighbor distances. Their calls are a series of pulses, and the pulse rate is

known to be important in mate recognition. In the Mate Recognition area of sympatry, P. ferriarum has a faster pulse rate À1 One of the most important decisions an animal can compared with allopatry, about 30 pulses s com- À1 make is with whom to mate. This single act can pared with 20 pulses s . This faster rate enhances ensure reproduction between individuals and the per- the difference between P. ferriarum and P. nigrita, À1 sistence of a genetic lineage. The mating call is the whose rate is about 20 pulses s whether these frogs are sympatric or allopatric with P. nigrita. A similar dominant cue used by males to advertise their pres- ence and identity to females, and females attend care- situation occurs in the Australian frogs Litoria ewingii fully to call attributes when choosing a mate. There is and L. verreauxii (Figure 6). Their pulse rates are similar in allopatry. But the calls of each species variation in mating calls among species, populations, and males within populations. Much of this signal differ between sympatry and allopatry. Specifically, variation is salient to a female and influences her in sympatry the L. ewingi call is slower (68 versus À1 choice of mates. 73 pulses s ) and the call of L. verreauxii is much À1 faster (138 vs. 84 pulses s ). In phonotaxis exp- Species recognition Species recognition occurs when eriments, the species can distinguish each other’s individuals recognize and prefer members of their calls in sympatry, but L. ewingii in sympatry cannot own species as mates over members of other species. distinguish its call from the similar calls of L. verauxii

As noted above, the frog’s auditory system is biased in allopatry. Thus not only have the calls of the two toward perceiving and responding to calls of their species diverged in sympatry, but these differences are own species in preference to calls of other species. salient to the receiver, and if the calls had not diverged

This functional correlation between sender and rein sympatry, there would be breakdown of species ceiver predicts that females should be able to dis- recognition. criminate easily among calls in favor of conspecifics. Most studies of reproductive character displace-

Phonotaxis experiments with numerous species have ment have concentrated on evolutionary changes in shown this to be the case. In addition, a number of the signal rather than the receiver, but the receiver can studies have used synthetic calls and systematically also respond to selection to better avoid calls of sym- deconstructed them to demonstrate the features salient patric heterospecifics. There are two species of gray to females. Two main points have emerged. Not all the treefrogs, Hyla chrysoscelis and H. versicolor, that acoustic detail is salient, and different species rely on are indistinguishable morphologically but differ in different constellations of call parameters for call rec- chromosome number (diploid and tetraploid) and ognition. An especially interesting example is mate the pulse pattern of their call (short pulses and long discrimination between two treefrogs Hyla cinerea pulses). H. chrysoscelis is usually allopatric with and H. gratiosa. These species co-occur throughout much of their range, and when they do so, their calls are more similar to one another than they are to any of L. e. the other local species. Females from each species are L. v. able to discriminate between the two calls, but they do so differently. H. cinerea uses spectral cues to make the discrimination whereas H. gratiosa attends mostly to temporal features.

If there is strong selection on females to mate with conspecific males rather than heterospecific ones, then the constellation of species at the breeding site should influence aspects of one another’s communication system. This phenomenon is known as re- L. e. productive character displacement, and its occurrence and L. v. has been perhaps best demonstrated by studies of frogs. These studies usually compare signal variation Figure 6 The geographic distributions of Litoria ewingii (L. e.) and L. verreauxi (L. v.) and the waveforms of their advertisement of two species in areas in which they do not co-occur calls. The two species are sympatric in the crosshatched area. (allopatry) and in areas where they do co-occur (sym- Modified from Halliday T (1980) Sexual Strategy (p. 74). Chicago: patry). Reproductive character displacement predicts University of Chicago Press.

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H. versicolor, and females prefer the longer-pulsed survival. In one study, male gray treefrogs that made calls produced by their males. When they are sympatric energetically more expensive calls were preferred by with H. versicolor , however, such a preference could females, and half-sib breeding experiments have increase their chances of mating with the wrong spe- shown that tadpoles of these males metamorphose cies. In sympatry, this preference for longer-pulsed calls faster and at larger size. This effect, however, is exhib- among conspecific males by H. chrysoscelis is signifi- ited only under certain ecological conditions. The cantly reduced. call, in this case, seems to advertise genetic variation

for at least some components of survival. Another Sexual selection Sexual selection by female choice type of genetically based choice is to shun matings occurs when female mating preference results in some with genetically similar males to avoid inbreeding. males in the population having greater reproductive In American toads, information about male related- success than others. The most thorough studies in ness is encoded in the calls, and females prefer calls of frogs show that (1) there is female choice of mates, less-related males. An analogous study in tu´ ngara (2) there is substantial variation in male mating suc- frogs, however, showed no such an effect. cess as a function of some aspects of the male’s pheno- A more recent hypothesis to explain female mate type, (3) there is a correlation between this aspect of choice is sensory exploitation. As mentioned above, the male’s phenotype and some aspect of his call, and, the response properties of the female’s auditory sys-

(4) those aspects of the call make the male more tem are biased toward acoustic parameters of the attractive to females in phonotaxis experiments. As species’ mating call. Males are under selection to an example, larger male tu´ ngara frogs in the wild have make their calls more attractive to females, and one greater mating success than smaller ones do, larger way to accomplish this is to evolve calls with acoustic males have lower-frequency calls because they have a parameters that exploit the females’ sensory, neural, larger larynx, and in phonotaxis experiments, females and cognitive biases. In tu´ ngara frogs, males always are more attracted to synthetic calls with lower fre- produce a whine whose dominant frequency matches quenciesthan to those with higher frequencies. the best excitatory frequency of the AP, and males can Females of species in addition to tu´ ngara frogs add up to seven secondary components or chucks prefer lower-frequency calls. Even more species prefer that stimulate the best excitatory frequency of the calls with faster pulse rates. A general theme is that BP. Males add chucks to their calls when they vocally females prefer more acoustic energy. They often tend compete with one another. Simple calls, whines only, to prefer faster calls, longer calls, higher-amplitude are both necessary and sufficient to attract females calls, and calls that stimulate one rather than two and elicit calling from other males. The chuck by itself peripheral end organs. A recurrent question ever is not salient to either sex, but the addition of chucks since Darwin is why females prefer some males over to a whine makes the whine more attractive to females others. One hypothesis is that females should choose and elicits more calling from males. There seems to be males who provide an immediate and direct benefit in nothing special about the chuck except that it stimu- reproductive success. There is good evidence for this lates the female’s auditory system. Other sounds, such in frogs. In some cases, females prefer males that as noise, tones, bells, and whistles, increase the whi- increase the number of offspring sired. In bullfrogs, ne’s attractiveness to the same degree as a chuck. larger males have territories that afford the eggs more Closely related species that do not produce a chuck protection from leech predation. In other cases, have the same BP tuning, so it seems clear that the females prefer larger males because they fertilize chuck and its dominant frequency evolved in tu´ ngara more eggs. This is not because of differences in frogs to stimulate the tuning of the inner ear organ sperm supply, however, but because there is mechani- that already existed. In addition, in some of these cally a better match of the male’s and female’s gonon- closely related species without chucks, females prefer pores during external fertilization. The better the the calls of their own species to which the chuck of a match, the more the sperm come into contact with tu´ ngara frog is added. As this short review of female the eggs. Females of some species, such as tu´ ngara choice shows, there are a number of different scenar- frogs, accrue this advantage in fertilization success ios that can favor the evolution of female choice through a simple preference for larger males, while among conspecifics, and these forces could act in others, such as the Australian frog Uperoleia rugosa, concert. choose males who are not only larger than average Eavesdroppers on Frog Communication by but of a specific size relative to the female’s own size. Predators Another hypothesis for the evolution of female choice is based on indirect benefits: Females should When animals communicate, there is, at minimum, a choose males whose genotypes are superior for sender and an intended receiver. But other animals

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selection. The former favors males that make conspic-

uous signals that are more attractive to females, but these more attractive calls are simultaneously selected against because of their low survival probabilities.

See also: Communication Networks and Eavesdropping in Animals; Communication in Terrestrial Animals; Game Theory and the Economics of Animal Communication; Multimodal Signaling in Animals; Seismic and

Vibrational Signals in Animals; Sexual Selection and the Evolution of Animal Signals; Signal Transmission in Natural Environments.

Further Reading Figure 7 The frog-eating bat Trachops cirrhosus capturing a calling male tu´ngara frog. Photo by Merlin Tuttle, Bat Conserva- Feng AS, Narins PN, Xu C-H, et al. (2006) Ultrasonic communication International. tion in frogs. Nature 440: 333–336. Fritzsch B, Ryan MJ, Wilczynski W, Hetherington TE, and Walkowiak W (eds.) (1988) The Evolution of the Amphibian might be listening to exploit the communication sys- Auditory System. New York: Wiley. tem. These other animals are called eavesdroppers. Gerhardt HC and Huber F (2002) Acoustic Communication in They are especially common in sexual communica- Insects and Anurans. Chicago: University of Chicago Press. Gridi-Papp M, Rand AS, and Ryan MJ (2006) Complex call pro- tion systems in which long-distance signals are loud duction in tu´ ngara frogs. Nature 441: 38. and conspicuous. Hoke KL, Burmeister SS, Fernald RD, et al. (2004) Functional The best known eavesdropper on frog calls is the mapping of the auditory midbrain during mate call reception. frog-eating bat Trachops cirrhosus (Figure 7). These Journal of Neuroscience 24: 11264–11272. bats feed on frogs, and in Panama they are especially Hoskin CJ, Higgie M, McDonald KR, and Moritz C (2005) Rein- fond of tu´ ngara frogs. These bats are especially sensi- forcement drives rapid allopatric speciation. Nature 437: 1353– 1356. tive to the relatively low-frequency sounds in frog Narins PM, Grabul DS, Soma KK, Gaucher P, and Ho¨ dl W (2005) calls, and they use the calls to localize the male. Like Cross-modal integration in a dart-poison frog. Proceedings female tu´ ngara frogs, these bats are attracted to of the National Academy of Sciences of the United States of simple, whine-only calls, and also like female tu´ ngara America 102: 2425–2429. Ryan MJ (1985) The Tu´ ngara Frog: A Study in Sexual Selection and frogs, they are more attracted to whines with chucks Communication. Chicago: University of Chicago Press. than to whines alone. A group of flies in the genus Ryan MJ (2001) Anuran Communication. Washington, DC: Smith- Corethrella shows analogous reactions to tu´ngara sonian Institution Press. frog calls. These flies take a blood meal from frogs; Waldman B and Bishop PJ (2004) Chemical communication in an they use the frog’s call for localization; and although archaic anuran. Behavioral Ecology 15: 83–93. the flies can locate males producing simple calls, they Welch AM, Semlitsch RD, and Gerhardt HC (1998) Call duration as an indicator of genetic quality in male gray tree frogs. Science are preferentially attracted to complex calls. These cases 280: 1928–1930. of eavesdropping illustrate nicely the conflict often seen Wilczynski W and Capranica RR (1984) The auditory system of in communication systems between sexual and natural anuran amphibians. Progress in Neurobiology 22: 1–38.

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